Download Impacts of Agriculture on Amphibians at Multiple Scales

Henna Piha
Henna Piha
HELSINKI 2006
EDITA
HELSINKI 2006
Impacts of Agriculture on Amphibians at Multiple Scales
ISBN 952-92-1163-5
Impacts of Agriculture
on Amphibians at Multiple Scales
Impacts of Agriculture on
Amphibians at Multiple Scales
Henna Piha
Ecological Genetics Research Unit
Department of Biological and Environmental Sciences
Faculty of Biosciences
University of Helsinki
Finland
Academic dissertation
To be presented, with permission of the Faculty of Biosciences of the University of
Helsinki, for public criticism in the Auditorium 1041 of Biocenter 2, Viikinkaari 5,
December 1st, at 12 o’clock noon.
Helsinki 2006
© Henna Piha (chapters 0, II, IV)
© American Chemical Society (chapter I)
© American Society of Ichthyologists and Herpetologists (chapter III)
© Blackwell Science (chapter V)
Author’s address:
Department of Biological and Environmental Sciences
P. O. Box 65 (Viikinkaari 1)
FI-00014 University of Helsinki
Finland
E-mail: [email protected]
ISBN 952-92-1163-5 (paperback)
ISBN 952-10-3472-6 (PDF)
http://ethesis.helsinki.fi
Layout Timo Päivärinta
Cover design and layout Päivi Puustinen
Edita
Helsinki 2006
Impacts of Agriculture on Amphibians at Multiple Scales
Henna Piha
This thesis is based on the following articles, which are referred to in the text by their
Roman numerals:
I
Teplitsky C, Piha H, Laurila A, Merilä J. 2005. Common pesticide increases costs
of antipredator defenses in Rana temporaria tadpoles. Environmental Science &
Technology 39:6079-6085.
II
Piha H, Laurila A, Merilä J. Pesticide effects on tadpoles: interactions with
predation risk and competition, and the importance of compensatory growth.
Manuscript.
III
Piha H, Pekkonen M, Merilä J. 2006. Morphological abnormalities in amphibians
in agricultural habitats: a case study of the common frog Rana temporaria. Copeia,
in press.
IV
Piha H, Luoto M, Sterner M, Merilä J. Amphibian occurrence in human-impacted
landscapes is influenced by current-day and historic landscape characteristics.
Manuscript.
V
Piha H, Luoto M, Piha M, Merilä J. 2006. Anuran abundance and persistence in
agricultural landscapes during a climatic extreme. Global Change Biology 12:112.
Contributions
I
II
III
IV
V
Original idea
HP, CT
AL
HP
HP
JM
HP
Study design
HP, CT
HP, AL
HP
HP, JM
ML
HP, MP
Data collection CT
HP
HP, MPe
JM, MS
HP
Methods &
analyses
HP, CT
HP
HP, MPe
HP, ML
HP, ML
MP
Manuscript
preparation
HP, CT
AL, JM
HP, AL
JM
HP, JM
HP, JM
ML
HP, JM
ML
Henna Piha (HP), Céline Teplitsky (CT), Anssi Laurila (AL), Juha Merilä (JM), Minna
Pekkonen (MPe), Miska Luoto (ML), Mattias Sterner (MS), Markus Piha (MP)
Supervisors
Prof. Juha Merilä, University of Helsinki, Finland
Research Prof. Miska Luoto, University of Oulu, Finland
Reviewers
Associate Prof. Rick Relyea, University of Pittsburgh, U.S.A.
Prof. David Skelly, Yale University, U.S.A.
Examiner
Dr. Josh Van Buskirk, University of Zurich, Switzerland
Abstract
Agriculture-mediated habitat loss and degradation together with climate change are
among the greatest global threats to species, communities, and ecosystem functioning.
During the last century, more than 50% of the world’s wetlands have been lost and
agricultural activities have subjected wetland species to increased isolation and
decreased quality of habitats. Likewise, as a part of agricultural intensification, the
use of pesticides has increased notably, and pesticide residues occur frequently in
wetlands making the exposure of wetland organisms to pesticides highly probable. In
this thesis, a set of ecotoxicological and landscape ecological studies were carried out to
investigate pesticide-effects on tadpoles, and species-habitat relationships of amphibians
in agricultural landscapes. The results show that the fitness of R. temporaria tadpoles
can be negatively affected by sublethal pesticide concentrations, and that pesticides may
increase the costs of response to natural environmental stressors. However, tadpoles may
also be able to compensate for some of the negative effects of pesticides. The results
further demonstrate that both historic and current-day agricultural land use can negatively
impact amphibians, but that in some cases the costs of living in agricultural habitats
may only become apparent when amphibians face other environmental stressors, such
as drought. Habitat heterogeneity may, however, increase the persistence of amphibians
in agricultural landscapes. Hence, the results suggest that amphibians are likely to be
affected by agricultural processes that operate at several spatial and temporal scales, and
that it is probable that various processes related to current-day agriculture will affect
both larval and adult amphibians. The results imply that maintaining dense wetland
patterns could enhance persistence of amphibian populations in agricultural habitats,
and indicate that heterogeneous landscapes may lower the risk of regional amphibian
population declines under extreme weather perturbations.
Contents
0 Summary
1. Introduction ............................................................................................................... 1
1.1. Expansion of agriculture ..................................................................................... 2
1.2. Intensification of agriculture ............................................................................... 3
1.3. Agriculture and climate change ........................................................................... 3
1.4. Amphibians and agriculture................................................................................. 6
1.5. Scales and approaches to studying agricultural impacts on amphibians ............. 7
2. Aims of the thesis ....................................................................................................... 9
3. Main results and discussion ...................................................................................... 11
3.1. Pesticide-effects on aquatic organisms .............................................................. 11
3.2. Pesticides and biotic stressors ............................................................................ 14
3.3. Role of habitat characteristics at multiple scales ............................................... 16
4. Conclusions .............................................................................................................. 18
5. Acknowledgements................................................................................................... 20
6. Literature cited.......................................................................................................... 22
I
II
III
IV
V
Introduction
Summary
1. Introduction
The expansion and intensification of
agricultural land use during the last
century are among the most predominant
human-induced changes in the global
environment (Matson et al. 1997, Tilman
et al. 2002, Green et al. 2005). Conversion
of natural habitats to croplands and
permanent pastures has reduced the
extent of natural habitats on agriculturally
usable land by more than 50% (Green
et al. 2005). Currently agriculture
represents the major form of land use
throughout most of Europe and North
America, where agricultural production
and productivity have intensified rapidly
over the past 60 years particularly due to
increased mechanization, irrigation and
agrochemical use (Matson et al. 1997,
Krebs et al. 1999, Green et al. 2005).
Despite this general trend, considerable
variation in the intensity of agriculture
exists among European countries.
Agricultural intensification is generally
higher in European Union (EU) member
countries than in non-EU member countries
mostly due to the Common Agricultural
Policy (CAP), which is a price-support
policy that subsidizes production and
keeps prices artificially high (Krebs et al.
1999, Donald et al. 2001). In Finland (EUmember since 1995), only 7% of the land
is covered by croplands. However, in the
main agricultural regions of southern and
western Finland, croplands cover roughly
30% of the land (Pitkänen & Tiainen
2000). Finnish agriculture has intensified
in accordance with other EU-countries,
major changes including decreased mixed
farming and dairy farming, increased
farm sizes, intensified land use, loss of
meadows, and increased agrochemical
use (Pitkänen & Tiainen 2000, Luoto et al.
2003; Fig. 1).
Figure 1. Trends in the total pesticide sales in Finland (Evira 2006).
AI = active ingredients.
1
Introduction
Although modern-day agriculture
has enabled the feeding of the world’s
growing population, concerns have risen
over its sustainability and environmental
consequences (Matson et al. 1997, Krebs
et al. 1999, Tilman et al. 2002, Green et
al. 2005). Expansion of agricultural land
has caused extensive habitat loss and
degradation, which are among the greatest
current and future threats to biodiversity
(Sala et al. 2000, Dirzo & Raven 2003).
Agricultural intensification has led to
widespread farmland biodiversity losses
in temperate areas (Krebs et al. 1999,
Donald et al. 2001, Benton et al. 2003), and
deterioration in soil, water and air quality
(Stoate et al. 2001, Tilman et al. 2002).
Farming is already the greatest extinction
risk to birds and during the next 50 years
global agricultural expansion is predicted
to cause unprecedented ecosystem
simplification, loss of ecosystem services,
and species extinctions (Tilman et al.
2001, Green et al. 2005). Additionally, the
negative impacts of modern-day agriculture
are likely to increase in combination with
climate change (Travis 2000, Opdam &
Wascher 2004). In the following, I shall
focus on three ecologically important
aspects of agriculture: (1) the impacts
of agricultural expansion on landscape
characteristics and different taxa (including
non-farmland species), (2) the impacts of
agricultural intensification, which chiefly
affect farmland species, but can also be
far-reaching (e.g. chemicalisation effects),
and (3) the combined effects of modernday agriculture and climate change.
1.1. Expansion of agriculture
The expansion of farmland areas has caused
destruction and loss of natural habitats
(e.g. wetlands, temperate grasslands,
forests) with detrimental impacts on many
species (e.g. Bakker & Berendse 1999,
2
Trzcinski et al. 1999, Lienert et al. 2002).
Currently wetlands are among the most
threatened ecosystems of the world, their
total area having declined by more than
50% in Europe and North America during
the last century largely due to agricultural
expansion (OECD 1996, Zedler & Kercher
2005). The domination of agricultural
land in relation to other habitat types
means that in agriculture-dominated areas,
all other habitats may be embedded in
agricultural land, thereupon increasing
fragmentation of natural habitats (i.e. loss
of habitat leading to a reduction in patch
size and increased patch isolation; Andrén
1994) and decreasing habitat quality
(e.g. Brinson & Alvarez 2002, McCauley
& Jenkins 2005). In smaller and more
isolated habitat fragments, species are
more prone to local extinctions and
population declines than in less fragmented
habitats as a consequence of diminished
population sizes and reduced colonization
and immigration rates (Andrén 1994,
Fahrig 2003, Ewers & Didham 2006). For
instance, increased isolation caused by
agricultural expansion has resulted in the
decreased abundance and species richness
of flower-visiting bees, and in impaired
plant-pollinator interactions (SteffanDewenter & Tscharntke 1999), whereas
agriculture-mediated forest fragmentation
has impacted negatively the occurrence
and reproductive success of forest birds
(Åberg et al. 1995, Bayne & Hobson
1997). Habitat loss and fragmentation can
also affect species through increased edge
effects (Fagan et al. 1999, Ries et al. 2004),
changes in the microclimate (Saunders et
al. 1991), and decreased genetic variation
(Young et al. 1996), the latter being
observed for example with common frog
Rana temporaria populations in areas
of intensive agriculture (Johansson et
al. 2005). Additionally, habitat loss may
Introduction
influence the potential of populations
to adapt in response to environmental
degradation (Stockwell et al. 2003),
and make them more sensitive to other
environmental stressors, such as climate
change (Travis 2000, Opdam & Wascher
2004).
Many of the negative impacts of
modern-day agriculture are related to
its effects on matrix quality (i.e. the
landscape surrounding suitable habitat
patches), particularly the heterogeneity
of the matrix (Benton et al. 2003, Opdam
& Wascher 2004, Donald & Evans 2006).
Matrix quality can be extremely important
in determining population dynamics and
ecosystem functioning in fragmented
landscapes (Fahrig 2001, Vandermeer &
Carvajal 2001). It can affect the ability
of species to attain resources, their
movement and dispersal abilities, and the
strength of edge effects, and hence, may
in some decrease the negative impacts
of fragmentation (Tscharntke et al. 2002,
Donald & Evans 2006, Ewers & Didham
2006). In areas of intensive agriculture,
landscape heterogeneity has benefited
various plant and animal species (e.g.
Weibull et al. 2000, Benton et al. 2003,
Johansson et al. 2005, Roschewitz et al.
2005). Likewise, heterogeneity among
agricultural habitats (i.e. between and
within fields) can be important for the
maintenance of biodiversity in farmland
ecosystems (Robinson & Sutherland
2002, Benton et al. 2003, Donald &
Evans 2006), but it is threatened more by
the intensification than the expansion of
agriculture, as will be discussed next.
1.2. Intensification of agriculture
Agricultural intensification includes
various spatial and temporal processes,
which aim at increasing crop yields per
unit area, but which have increased the
homogeneity of agricultural habitats, and
caused increased soil erosion, and water
and air pollution (Stoate et al. 2001, Benton
et al. 2003; Table 1). Negative impacts
of agricultural intensification have been
demonstrated in many species (Table 1),
most of all in farmland birds, which are
by far the most studied taxa (reviews in
Stoate et al. 2001, Robinson & Sutherland
2002, Benton et al. 2003, Newton 2004).
The impacts of agricultural intensification
are complex and often difficult to identify,
as the different processes can interact
and affect organisms both directly and
indirectly (Robinson & Sutherland 2002,
Benton et al. 2003). The main effects of
agricultural intensification on farmland
species can be coarsely divided into two
groups: those resulting from changes in
the availability and quality of breeding
and foraging habitats, and those resulting
from changes in farmland communities
(e.g. Krebs et al. 1999, Donald et al. 2001,
Newton 2004; Box 1).
1.3. Agriculture and climate change
Although the impacts of agricultural
expansion and intensification on species
extend far beyond farmland areas, a key
driving force of species’ distributions at
large biogeographical scales is climate.
Human-induced climate change (caused
by increased concentrations of greenhouse
gases) involves increases in the mean
global temperature, changes in the
distribution and frequency of precipitation,
and increases in the frequency of extreme
climatic events, such as droughts and
floods (Easterling et al. 2000, Hughes
2000). Global warming has been related
to alterations in the distribution and
phenology of various taxa, and to changes
in the composition and interactions within
communities (Hughes 2000, Walther et
al. 2002, Parmesan & Yohe 2003, Root
3
4
Reduction in species diversity by killing weeds and favoring
competitive grass species through drainage and fertilizer use
Increased uniformity of establishment and growth, reduced
species and structural diversity of vegetation, pollution of soil, air,
and ground and surface waters
More uniform establishment and crop growth, increased erosion,
decreased water supplies
Grassland improvement
Increased agrochemical
use
Increased drainage and
irrigation
1.
2.
3.
4.
5.
6.
Blanco et al. 1998
Robinson & Sutherland 2002
Atkinson et al. 2002
Peach et al. 2004
Dennis et al. 1994
Holland & Fahrig 2000
19.
20.
21.
22.
23.
Davidson 2004
Tew et al. 1992
Stoate et al. 2001
Diekotter et al. 2006
Johansson et al. 2005
Negative impacts on bird and invertebrate abundances (3, 10,
21), potential threat to bumblebees (22), and amphibians (23)
Negative effects on birds (10), butterflies (15), arthropod
communities (12, 16-18), amphibians (19), and wood mice (20)
Negative impacts on the diversity and abundance of birds (3,
11), dung beetles (12), true bugs (13), and bumblebees (14)
Declines of various bird species (9, 10)
Declines of bird species (4), arthropods (5, 6), weed diversity
(7), and amphibians (8)
Negative associations with bird distributions (3)
Negative associations with habitat availability and density of
several farmland bird species (1, 2)
Effects on species
Di Giulio et al. 2001
Croxton et al. 2002
Longley & Sotherton 1997
Chiverton & Sotherton 1991
Sotherton 1998
Haughton et al. 1999
More uniform swards, and more fields in the same management
state at any one time, stubbles available for only short periods
Mechanization
13.
14.
15.
16.
17.
18.
Loss of semi-natural habitat features, such as ponds, noncropped field margins and scrub
Removal of
uncultivated areas
De Snoo 1999
Vos & Stumpel 1995
Chamberlain et al. 2000
Newton 2004
Vickery et al. 2001
Hutton & Giller 2003
Larger blocks of land under the same agriculturally productive
management at any given time and for longer periods
Simplified crop
rotations
7.
8.
9.
10.
11.
12.
Domination of fewer larger farm units and larger contiguous
areas under common management systems and/or crop
rotations
Farm unit consolidation
and specialization
Cited references:
Consequence for agricultural habitats
Process
Table 1. Consequences and effects of different processes of agricultural intensification on habitats and species (classification of processes adapted
from Benton et al. 2003).
Introduction
Introduction
Box 1. Examples of the main ways in which agricultural intensification can
affect species. Group 1 = changes in habitat availability and quality; Group
2 = changes in farmland community structure and functioning.
Group 1: Loss of semi-natural habitats
The loss of semi-natural habitats has had wide-ranging impacts on terrestrial
and aquatic species alike. The removal of field boundaries and uncultivated
areas, for instance, has led to the loss of suitable terrestrial breeding and
foraging habitats for many species, whereas the drainage and filling of ponds
has significantly decreased the availability of small wetlands (e.g. Beebee
1983), which often support diverse aquatic communities (Oertli et al. 2002,
Nicolet et al. 2004, Williams et al. 2004) and are important habitats for many
farmland birds (Newton 2004, Bradbury & Kirby 2006). The remaining aquatic
habitats are also likely to experience a decrease in quality caused by
agricultural intensification (e.g. grazing disturbance, nutrient and pesticide
runoff; Knutson et al. 2004, Declerck et al. 2006), which may reduce their value
for farmland diversity (Bradbury & Kirby 2006) For discussion on pesticideeffects in aquatic habitats see 3.1.
Group 2: Pesticide-mediated changes in food webs
A classical example of agriculture-mediated changes in food webs is the impact
of pesticide-use on partridge populations in the U.K. (Green 1984, Rands 1985).
It was shown that the use of herbicides decreased the abundance of weeds,
which resulted in decreased arthropod abundances, which in return caused
impoverished food supplies for partridge chicks (Chiverton & Sotherton 1991).
These changes led to increased chick mortality and consequent population
declines (Green 1984, Rands 1985, Potts & Aebischer 1995). The use of
insecticides has also been shown to depress breeding productivity of birds by
decreasing insect food abundances (Hart et al. 2006), and in Scotland, a link
between arthropod abundances, farmland birds and agricultural practices has
recently been clearly shown (Benton et al. 2002). For discussion on pesticideeffects on the functioning of aquatic communities see 3.2.
et al. 2003), whereas climatic extremes
have been shown to cause synchronized
population crashes and extinctions (e.g.
Thomas et al. 1996, Sutcliffe et al. 1997,
Hawkins & Holyoak 1998). The impact
of climate change on the abundance and
persistence of species can be affected by
habitat loss. Firstly, the shifting of species
ranges in response to climate change may
be blocked in areas where the degree of
habitat fragmentation is below the level
required for population persistence, and
secondly, the increased frequency of largescale disturbances caused by climatic
extremes may cause increasing gaps and
an overall contraction of distribution
ranges (Warren et al. 2001, Opdam &
Wascher 2004). Habitat heterogeneity can
to increase population persistence under
variable climatic conditions (Weiss et al.
1988, Kindvall 1996, McLaughlin et al.
2002), but as modern-day agriculture causes
both habitat loss and homogenization, it
is likely that in agricultural landscapes,
species may be particularly sensitive to
climate change (Travis 2002, Donald &
Evans 2006).
5
Introduction
1.4. Amphibians and agriculture
In recent studies on the effects of
agricultural intensification on biodiversity,
amphibians have usually been brushed
aside (e.g. Stoate et al. 2001, Robinson
& Sutherland 2002, Hole et al. 2005).
This is surprising, as among amphibian
researchers, various processes related to
agricultural intensification are regarded
as major threats to amphibian individuals
and populations (e.g. Joly et al. 2001,
Linder et al. 2003, Semlitsch 2003,
Knutson et al. 2004, Relyea et al. 2005),
and to be partly responsible for global
amphibian population declines (Box 2).
In the following, I shall illustrate how
and why amphibians may be affected by
modern-day agriculture, and some of the
approaches to studying the impacts of
agricultural intensification on amphibians.
Amphibians are an extremely diverse
vertebrate class with large variation in
physiological, behavioral, morphological
and ecological characteristics (Feder &
Burggren 1992). In the following, when
speaking of amphibians, I refer to species
which employ a general life history strategy
entailing the use of aquatic habitats for
reproduction and larval development, and
terrestrial habitats for growth to maturation
and dispersal. I also restrict my discussion
primarily to pond-breeding species (i.e.
amphibians which use lentic aquatic
habitats such as pools, ponds, lakes, and
marshes for breeding) living in temperate
regions, because all my work has been
conducted with such species, and they are
the most common type of amphibians in
Europe and North America with important
roles in ecosystems (Box 3).
Pond-breeding amphibians require
both aquatic and terrestrial habitats, and
are hence subject to alterations in the
availability and/or quality of either habitat
type (Semlitsch 2000). Consequently, they
are likely sensitive to habitat loss caused by
agricultural expansion (Laan & Verboom
1990, Hecnar & M’Closkey 1998,
Houlahan & Findlay 2003), to increased
isolation of breeding and foraging habitats
(increased survival risks related to longer
migrations and distances to neighboring
source populations in a possibly hostile
matrix; e.g. Gibbs 1993, Joly et al. 2001,
Rothermel & Semlitsch 2002), and to the
decreased quality of breeding sites (e.g.
Cooke 1981, Knutson et al. 2004, Declerck
et al. 2006). Additionally, the reduced
amount of ditches caused by increased
subsurface drainage can hinder amphibian
movement (Reh & Seitz 1990, Pope et al.
2000, Mazerolle 2004).
Box 2. Global amphibian population declines.
Currently approximately one third of the world’s amphibian species are
threatened and at least 43% of all species have declined (Stuart et al. 2004).
Habitat loss and degradation are among the greatest threats to many of the
declining populations, but additional threats include pesticides and other
chemical pollutants, increased UV-B radiation, climate change, introduced
predators, diseases, and exploitation (Collins & Storfer 2003, Beebee & Griffiths
2005, Pounds et al. 2006). Additionally, findings of amphibian populations with
unexpectedly high incidences of morphological abnormalities have been made
particularly in the U.S. (Blaustein & Johnson 2003, Sessions 2003). It is likely
that the stressors are not working independently, but interactions amongst them
may be the most likely threat to many species (e.g. Kiesecker et al. 2001,
Blaustein & Kiesecker 2002, Pounds et al. 2006).
6
Introduction
Several intrinsic and extrinsic factors
increase the likelihood of amphibians being
sensitive to agricultural intensification.
Firstly, many amphibian species have
strong annual population fluctuations
(Pechmann et al. 1991, Meyer et al. 1998,
Trenham et al. 2003), high site fidelity
(Smith & Green 2005), and relatively
weak dispersal abilities (Sinsch 1990,
but see Smith & Green 2005), which
may make them particularly sensitive to
isolation effects. Secondly, they have semipermeable skins which protect them weakly
against contaminants and drying (Feder
& Burggren 1992). They are particularly
likely to be exposed to pesticides during
the aquatic development, as it coincides
with the timing of pesticide use. For
example, species of the ranid frogs in the
U.S. breed sequentially throughout the
spring and summer, and breeding periods
may extend over periods of many weeks.
Hence it is very likely that at least some of
the species will be exposed to pesticides
(Berrill et al. 1994). Furthermore, because
aquatic habitats are the ultimate sinks for
most chemical contaminants regardless of
their source, aquatic stages of amphibians
are likely exposed even if the breeding
sites are not situated within agricultural
landscapes. However, exposure to
pesticides during terrestrial development
may likewise pose a threat for amphibians
(e.g. Relyea 2005).
1.5. Scales and approaches to studying
agricultural impacts on amphibians
The problems and impacts of scale have
long been central issues in ecological
studies (Wiens 1989, Levin 1992). Each
individual and species experiences the
environment at a unique range of scales,
and different processes are likely to
be important on these different scales
(Levin 1992). Generally climate is
expected to govern organisms’ responses
at broad biogeographical scales whereas
land cover and biotic interactions are
considered to dominate at finer spatial
resolutions (Parmesan 1996, Pearson
et al. 2004, Luoto et al. 2006). Due to
this, and because agriculture operates at
several spatiotemporal scales, no single
measure can explain amphibian responses
to agricultural intensification (Burel et
al. 2004). Therefore, when studying the
impacts of agriculture on amphibians,
incorporation of multiple spatial and
temporal scales as well as different
approaches is necessary.
Box 3. Important ecosystem roles of pond-breeding amphibians (adapted
from Petranka & Kennedy 1999, Semlitsch 2003).
Larval anurans (frogs and toads) are both microphagous suspension feeders
(consuming e.g. pollen, algae, periphyton, microorganisms, and -zooplankton)
and macrophagous predators (consuming e.g. macroinvertebrates, amphibian
eggs, hatchlings and tadpoles), whereas larval caudates (salamanders and
newts) generally only consume secondary production. Terrestrial adults feed on
small invertebrates often not available to other vertebrate groups. Pondbreeding amphibians comprise a large amount of protein biomass that is
available in the food chain (e.g. for snakes, birds, and mammals) and serve as
nutrient vectors connecting aquatic and terrestrial environments through
emigration and immigration processes.
7
Introduction
Choice of scale
Firstly, effects of agricultural intensification
can be studied at the scale of the individual,
population, community or ecosystem.
Individual-based studies make possible
the investigation of specific mechanisms,
whereas studies at the population-level
or higher take into account impacts on
population dynamics, species-interactions,
and ecosystem functioning, which cannot
be estimated from individual-based
studies. Secondly, it is probable that
different developmental stages experience
the environment on different scales
(Levin 1992), and amphibians with their
biphasic lifestyles are a good example
of this. Hence, it is likely that different
processes of agricultural intensification
are important for the aquatic than for
the terrestrial life stages (see 1.4.), and
this should be acknowledged when
planning investigations. Thirdly, the
scale-dependence of different agricultural
processes (Benton et al. 2003) makes it
likely that amphibian populations will be
affected by agricultural processes operating
at both local and landscape levels. When
making choices regarding the levels to
study, it is worth remembering that when
moving from small scale approaches
to large scale approaches (spatial and
temporal) one has to trade off the loss of
detail for the gain of generality (Levin
1992).
Choice of approach
To study the effects of agricultural
intensification on amphibians, it is possible
to carry out experimental (manipulative)
or observational (mensurative) studies
8
(Hurlbert 1984). Pesticide-effects are
often studied using larval amphibians
(see 2.1.) and by conducting manipulative
experiments. The venue can be laboratory,
mesocosm, or field. Laboratory experiments allow the isolation of effects
of particular mechanisms, whereas
mesocosm and field experiments are
subject to environmental variability and
are structurally more complex, hence
allowing the prediction of effects on
natural populations and ecosystem-level
features (Kimball & Levin 1985, Skelly &
Kiesecker 2001). Laboratory experiments
are generally expected to yield the more
precise estimates of responses compared
to mesocosm and field studies, however,
this difference may not always be apparent
(Skelly & Kiesecker 2001). Impacts of
habitat composition and configuration
are generally approached by means of
observational studies. The benefit of
observational studies is that they have
high realism and generality, because
they are applied to unmanipulated, realworld systems. However, the results
are correlative and cannot be used to
distinguish cause from effect (McGarigal
& Cushman 2002). Outside of the breeding
season, adult amphibians are tedious to
study. Hence, most studies investigating
amphibian distributions, abundance and
diversity are conducted by studying
breeding pond assemblages. This enables
observations to be made at large scales, but
more detailed studies are needed to gain
information of e.g. amphibian migration
and small-scale habitat characteristics
important for the terrestrial stages.
Aims of the thesis
2. Aims of the thesis
The aim of my thesis was to study impacts of
agricultural intensification on amphibians
at multiple scales. Firstly, by studying
common frog Rana temporaria tadpoles,
I wanted to examine how fenpropimorph,
a commonly used morpholine fungicide,
may affect the fitness of tadpoles, and their
ability to cope with natural stressors (I-II;
Fig. 2). Secondly, by studying breeding
populations of four amphibian species
(common frog Rana temporaria, moor
frog Rana arvalis, common toad Bufo bufo,
smooth newt Triturus vulgaris), I wanted
to examine which habitat characteristics
impact the abundance, distribution and
persistence of these species (IV, V), and
the morphological development of R.
temporaria tadpoles in agricultural areas
(III; Fig. 2). Hence, I aimed to understand
how processes related to agricultural
expansion and intensification may affect
both the aquatic and terrestrial stages
of amphibians. I studied these issues by
applying ecotoxicological (I-III) and
landscape ecological (III-V) approaches,
and by conducting laboratory (I), outdoor
mesocosm (II), and observational field
studies in southern Finland (III, V; Fig. 3)
and on the Island of Gotland, Sweden (IV;
Fig. 3).
Recruitment
LARVAE &
METAMORPHS
Fitness & survival
Occurrence, persistence METAMORPHS
& ADULTS
& development
Pesticides I-III
Reproduction
Aquatic habitat IV
Predation I,II
Competition II
Landscape
characteristics III-V
Land use history IV
Climate V
Figure 2. The response variables (gray box), explanatory variables (open box), and amphibian
life stages studied in the thesis.
9
Aims of the thesis
Figure 3. The study areas used in articles III-V and the locations of the study sites. A = southern
Finland, B = Swedish island of Gotland.
10
Main results and discussion
3. Main results and discussion
The main study questions and main results
of the five articles are summarized in Table
2. In the following, I shall discuss these
results and their broader significance with
respect to published literature.
3.1. Pesticide-effects on aquatic
organisms
Organisms living in aquatic habitats
are likely exposed to a wide range of
contaminants via water, sediment, and
food (Farrington 1991). At concentrations
occurring in natural habitats, many
contaminants are lethal to freshwater
organisms, such as fish (Lemly 2002,
Hopkins et al. 2004), amphibians (Berrill
et al. 1998, Harris et al. 1998a, Boone
& James 2003), invertebrates (Schulz
& Liess 1999), and microorganisms
(DeLorenzo et al. 2001, Hanazato
2001; for a comprehensive database on
pesticide toxicity to aquatic species see
PAN Pesticides Database http://www.
pesticideinfo.org). Long-term exposure
to fenpropimorph at concentrations
occurring in natural habitats (11 μg/L) was
highly lethal to Rana temporaria tadpoles
(I). However, it is likely that tadpoles are
not exposed to such high concentrations
chronically in nature. Chronic exposure
to considerably lower fenpropimorph
concentrations (2 μg/L) nevertheless
reduced metamorphic size (I), and under
pulse exposure it slowed the tadpoles’
growth and development (II). Time to and
size at metamorphosis are important fitness
characteristics of amphibians, as they
are positively correlated to adult growth,
survival and reproductive success (Smith
1987, Semlitsch et al. 1988, Berven 1990,
Semlitsch & Gibbons 1990, Altwegg &
Reyer 2003). Large size at metamorphosis
can also benefit physiological and
locomotor performance in terrestrial
environments (Pough & Kamel 1984,
Goater et al. 1993), and high development
rates enable tadpoles to metamorphose
before habitats dry up (Smith 1983,
Newman 1988, Laurila & Kujasalo 1999,
Loman 2002), which is a likely threat for
tadpoles developing in temporary habitats
in agricultural landscapes. These results (I,
II) together with other amphibian studies
showing similar sublethal pesticide-effects
(reduced larval growth and development:
Berrill et al. 1998, Rohr et al. 2003,
Broomhall 2004, Relyea 2004a; increased
age and decreased size at metamorphosis:
Fioramonti et al. 1997, Bridges 2000,
Sullivan & Spence 2003) suggest that
current agriculture-related pesticide use
can pose a threat to amphibian populations
in the wild by decreasing the fitness of
individuals.
The negative effects of pesticides on
organisms can result from accumulation
(Sparling et al. 2001), metabolic changes
(e.g. elevated standard metabolic rates;
Weber 1996, Rowe et al. 2001), and
physiological effects (e.g. immune toxicity;
Galloway & Handy 2003, Gendron et al.
2003). Also behavioral changes (activity,
predator avoidance, feeding) are caused
by many pesticides (Cooke 1971, Weber
1996, Bridges 1997, Berrill et al. 1998).
Fenpropimorph affected the behavior
of R. temporaria tadpoles negatively by
decreasing their activity (I, II), which
likely explains part of the negative effects
observed on metamorphic size (I). Stressoreffects may not, however, be directly
apparent, but be seen as negative carryover effects at a later stage of development
(Bridges 2000, Pahkala et al. 2003, Rohr et
al. 2006a). Alternatively, when exposure to
a stressor is not chronic, individuals may
11
12
V
IV
III
II
I
In 2002, abundance was best explained by local habitat characteristics (amount of
ditches and ponds). In 2003, regional (water level) and landscape (forests) were positive
determinants of abundance, whereas field area (landscape level) correlated negatively.
The populations decreased less in areas where the change in water levels was smaller
and where habitat heterogeneity and coverage of urban areas at the landscape scale
were higher.
What is the role of habitat structure on population
persistence during an extreme drought?
Species responded rather similarly to different spatial scales of the landscape. The
effects of historic landscape characteristics were generally observed at larger spatial
scales than those of current-day landscape.
Are the effects of landscape characteristics in explaining
amphibian occurrence scale and/or species dependent?
Which local, landscape and regional habitat characteristics
explain R. temporaria abundance in agricultural areas
during a normal (2002) vs. a drought year (2003)?
Amphibian occurrence was best explained by local habitat characteristics, however
historic landscape characteristics generally explained as much of the variation in
response variables as current-day landscape characteristics. Agricultural land use (both
current-day and historic) was negatively associated with species’ occurrences.
No significant differences were observed among the different types of habitats (field,
grassland, forest).
Does the abnormality frequency differ among different types
of agricultural habitats?
How do local habitat, and current-day and historic
landscape characteristics explain amphibian occurrence and
species richness in agricultural areas of Gotland?
The frequency of morphological abnormalities in metamorphs did not differ from the
expected background frequency, abnormalities occurring in only 1.0% of the 4115
studied individuals.
Although FEN had negative synergistic and additive effects with predation risk and
competition on tadpoles, by metamorphosis the effects had largely disappeared, likely
due to compensatory growth of the tadpoles.
Does FEN increase the costs of responding to predation risk
and competition?
Does the abnormality frequency in R. temporaria
populations differ from the expected background frequency
of 0-5% in agricultural areas?
FEN impeded the tadpoles from increasing their activity in response to competition under
predation risk. Morphological responses were not impeded.
Does FEN impede the inducible responses of tadpoles to
predation risk and competition?
At 2 μg/L, the costs of antipredator defenses (decreased size, prolonged development)
were higher than in the absence of FEN.
Does FEN increase the costs of responding to predation
risk?
Tadpoles metamorphosed at a smaller size from the high FEN treatment when
competition was low, but not at other densities.
FEN did not impede behavioral or morphological responses to predation risk.
Does FEN impede inducible responses to predation risk?
Do predation risk and competition alter the effects of FEN
on R. temporaria tadpoles?
FEN decreased the tadpoles’ activity, growth and development rate. At 11 μg/L, FEN was
highly lethal, whereas at 2 μg/L, FEN decreased the size of the metamorphs.
Main results
Are environmentally realistic fenpropimorph (FEN)
concentrations harmful to Rana temporaria tadpoles?
Main study questions
Table 2. Summary of the main study questions and results of the five articles included in the thesis.
Main results and discussion
Main results and discussion
be able to compensate for the negative
effects on growth with compensatory
growth (Ali et al. 2003). Compensation
of negative pesticide-effects has been
shown at the population level (e.g. Forbes
et al. 2001, Hooper et al. 2003), however,
compensation at the individual level
following pesticide exposure has received
less attention in amphibian studies. Such a
response was present with R. temporaria
tadpoles, which compensated for the
negative effects of fenpropimorph on
growth so that by metamorphosis, these
effects had mostly disappeared (II).
These results imply that organisms may
be able to compensate for some of the
adverse effects of pesticides, and illustrate
the importance of taking into account
several endpoints for measuring effects
of toxicants on the fitness of individuals.
However, it should be acknowledged that
compensatory growth can also impose
costs for organisms, such as adverse
effects on later growth, reproduction or
survival (Metcalfe & Monaghan 2001, Ali
et al. 2003, Mangel & Munch 2005).
Contaminants can also cause
abnormal development in organisms.
In laboratory experiments, sublethal
levels of various pesticides have caused
developmental
abnormalities
(e.g.
visceral, mouth, eye and limb deformities)
in embryos and larval amphibians (e.g.
Alvarez et al. 1995, Harris et al. 1998a,
Bridges 2000, Greulich & Pflugmacher
2003, Rohr et al. 2003), and multiple
mechanisms exist whereby pesticides
may elicit demasculinizing effects in nontarget organisms (LeBlanc et al. 1997, see
Hayes et al. 2002). Increased frequencies
of developmental abnormalities have been
observed in amphibians in agricultural
habitats and in relation to agricultural
land use in the U.S., Canada, and Britain
(Cooke 1981, Ouellet et al. 1997, Bishop
et al. 1999, Hayes et al. 2002, Taylor et al.
2005). In Europe, recent knowledge of the
incidence of developmental abnormalities
is largely lacking (Ouellet 2000), and no
large-scale studies on the occurrence of
amphibian abnormalities in agricultural
landscapes had previous to study III been
carried out. In the agricultural habitats
of southern Finland, abnormalities were
not exceptionally high in R. temporaria
metamorphs, abnormalities occurring in
only 1% of the studied individuals (Table
2, III). These results together with reports
of low abnormality frequencies in some
farmland areas in the U.S. (Harris et al.
1998a, 1998b, Gillilland et al. 2001)
suggest that it is perhaps too early to say
that amphibians would generally be at
greater risk of obtaining abnormalities in
agricultural habitats than in other types
of landscapes. More studies at large
geographical and longer temporal scales
combined with water sample analyses
should be carried out in agricultural habitats
for a comprehensive understanding of this
phenomenon. Meanwhile, it is important
to remember that the negative effects
of pesticides can be manifested through
other paths (sublethal and lethal, direct
and indirect; discussed in 3.1. and 3.2.),
and hence developmental abnormalities
should not be used as the sole indicators
of pesticide-effects. It is also probable that
other factors, such as Ribeiroia parasites
(Johnson et al. 2002, 2003) or UV-B
radiation (Pahkala et al. 2001, Ankley
et al. 2002) are responsible for some of
the cases where increased frequencies of
abnormalities have been observed.
A major challenge in estimating the
impacts of pesticides on organisms is
that the effects depend on various factors
such as chemical characteristics (dose; I,
II, mode of action), characteristics of the
organisms (species, life stage, size), and
13
Main results and discussion
context (other environmental factors; I,
II), see reviews (in DeLorenzo et al. 2001,
Hanazato 2001, Rohr et al. 2006b). The
combined effects of pesticides and other
contaminants (MIX), or pesticides and
biotic stressors (BIO) to species of aquatic
communities may be additive (MIX:
Fairchild et al. 1994, Relyea 2004a; BIO:
Sibly et al. 2000, I, II), antagonistic (MIX:
Hoagland et al. 1993; BIO: Sibly et al.
2000, Hooper et al. 2003), or synergistic
(MIX: Howe et al. 1988, Anderson &
Lydy 2002; BIO: Hanazato 1999, Relyea
& Mills 2001, Kiesecker 2002, Relyea
2003a, I, II). From this follows that in
nature, contaminants may lead to complex
indirect effects, which modify species
interactions and population, community
and ecosystem functioning (Hanazato
2001, Fleeger et al. 2003, Rohr et al.
2006b, see also 1.2.). As importantly,
contaminants may interfere with the ability
of organisms to adapt to natural variations
in their environment (e.g. Barry 2000)
which may lead to population declines
and altered community functioning (alike
described above). In the following, I shall
discuss possible effects of pesticideexposure on the ability of individuals to
cope with predation and competition.
3.2. Pesticides and biotic stressors
Larval anurans often develop in
environments where the levels of
predation and competition are variable and
unpredictable (e.g. Wilbur 1980). Under
such circumstances, phenotypically plastic
responses in behavior and morphology
protect organisms against biotic stressors
and enhance their fitness (Tollrian &
Harvell 1999, Box 4). Pesticides may,
however, alter the effects of predation and
competition on organisms and vice versa,
or organisms’ ability to respond to these
stressors. Fenpropimorph decreased the
14
activity of R. temporaria tadpoles (I, II),
and hence did not impede their behavioral
response to predation stress (Box 4).
However, fenpropimorph impeded the
tadpoles from responding to competition
in an adaptive way, as they were unable to
increase activity as a response to increasing
competition when experiencing predation
risk (Box 4, II). Hence, synergistic negative
effects on adaptive plastic responses were
observed.
The effects of pesticides on
phenotypic plasticity have thus far
remained largely unstudied. However, the
few studies investigating pesticide-effects
on phenotypic plasticity have shown that
pesticides can inhibit the development of
neckteeth in Daphnia in response to predation threat (Barry 2000). Additionally,
the costs of responding to biotic stressors
may increase under pesticide stress
(Hanazato 1999, Barry 2000, Hanazato
2001). Also fenpropimorph increased
the costs of responding to predation risk,
which could be seen as a decreased relative
size of the tadpoles and increased time to
metamorphosis (I). These results imply
that in contaminated habitats organisms
may have lowered fitness due to impeded
adaptive responses to environmental
factors, or to increased costs of responding
to the factors. Considering that pesticides
may also increase susceptibility to predation
(Cooke 1971, Verrell 2000, Schulz &
Dabrowski 2001, Broomhall 2004)
and that the lethality of pesticides may
increase when combined with predation
risk (Relyea & Mills 2001, Relyea 2003a)
it is presumable that pesticides can pose a
threat to amphibians also at the population
level (Sih et al. 2004a, 2004b, but see
Schmidt 2004). Nonetheless, it should be
remembered that at the community level,
interactions between pesticides and biotic
factors may result in complex changes in
Main results and discussion
Box 4. Induced responses of tadpoles to predation and competition.
Typical responses of tadpoles to predation risk are altered behavior (decreased
activity, increased hiding, altered microhabitat use;1-4, I, II) and/or morphology
(development of relatively small bodies and deep tails;5-7, I, II).These
responses increase the likelihood of survival in predator-environments (e.g.
improved escape ability; 8, decreased encounter rates; 1) but may include
costs, such as decreased growth and development rate (2, 6, 9-13, I, II),
delayed maturity or reduced fecundity (14), increased energetic swimming costs
(15), and lowered survival in the absence of predation (8). The costs may arise
from various factors, such as maintenance and production of induced defenses
(16), and shifts in allocation of time and energy (13). Tadpoles can modify their
responses according to the diet of the predators (stronger responses when
conspecifics killed; 17, 18), and to the amount of prey eaten or number and/or
type of predators present (19-22). Their responses can also depend on their
development stage (23), and their phenotypic strategy can change over
ontogeny and be reversible in response to predator presence and absence (7).
Competition generally induces increased activity (3, 24, 25, II), which results in
more encounters with food and hence results in higher energy gain that
translates to higher growth rate and larger size (26). Tadpoles also respond to
competition with morphological responses, such as relatively large bodies, wide
mouth parts and small tails (27-29, II). These plastic responses increase the
tadpoles’ competitive ability, but may increase their risk of being preyed upon
(3, 28). When confronted with predation and competition, organisms generally
face a trade-off situation between predator resistance ability and competitive
ability (30), as competition and predation often induce traits in opposite
directions (28, 31, 32, II).
Cited references:
1. Kats et al. 1988
2. Skelly & Werner 1990
3. Anholt & Werner 1995
4. Laurila 2000
5. Lardner 2000
6. Van Buskirk 2002
7. Relyea 2003b
8. McCollum & Van Buskirk 1996
9. Skelly 1992
10. Smith & Van Buskirk 1995
11. Relyea & Werner 1999
12. Altwegg 2002
13. Van Buskirk 2000
14. Dahl & Peckarsky 2002
15. Petterson & Brönmark 1997
16. DeWitt et al.1998
17. Laurila et al. 1997
18. Kiesecker et al. 2002
19. Laurila et al. 2002
20. Van Buskirk & Arioli 2002
21. Relyea 2003c
22. Teplitsky et al. 2004
food resources and predator-prey dynamics
(Boone & Semlitsch 2003, Boone et al.
2004, Mills & Semlitsch 2004, Relyea
et al. 2005, Rohr & Crumrine 2005) in
having positive effects on some species
whereas negative on others. Positive
effects on tadpoles include predatorrelease (occurring when predators are
23. Laurila et al. 2004
24. Anholt & Davies 1987
25. Anholt & Werner 1998
26. Werner & Anholt 1993
27. Relyea 2000
28. Relyea 2002
29. Relyea & Hoverman 2003
30. Lima & Dill 1990
31. Werner & Anholt 1996
32. Relyea 2004b
more vulnerable to pesticide exposure than
tadpoles; Boone & Semlitsch 2003, Mills
& Semlitsch 2004, Relyea et al. 2005),
and increased food resources (Boone
& Semlitsch 2002, Boone et al. 2004).
Whereas, by decreasing algal abundance
pesticides may exacerbate the effects of
competition (Mills & Semlitsch 2004).
15
Main results and discussion
3.3. Role of habitat characteristics at
multiple scales
Spatial scale
In general, organisms are expected
to favor environments in which their
survival and reproductive success is
maximized. Because the amphibian life
history includes aquatic and terrestrial
stages, it is not surprising that both local
and landscape scale characteristics have
been shown to be important determinants
of amphibian distributions (e.g. Mazerolle
& Villard 1999, Joly et al. 2001, Knutson
et al. 2004, Van Buskirk 2005, IV, V).
In Gotland, in landscapes modified by
agriculture, local pond characteristics
were stronger determinants of amphibian
occurrence and species richness than
landscape characteristics (IV). Canopy
cover of the shoreline was positively
associated with the occurrences of Rana
arvalis and Triturus vulgaris, and R.
arvalis and Bufo bufo were more likely
to occur in ponds which were small, deep
and scarcely vegetated, than in large,
shallow, and densely vegetated ponds. The
latter relationships likely reflect effects of
hydroperiod, the species avoiding habitats
which may dry up before the tadpoles
have had time to metamorphose. Many
amphibian species avoid ponds that contain
predatory fish (Kats et al. 1988, Wellborn
et al. 1996, Hecnar & M’Closkey 1998). In
Gotland, amphibians occurred more likely
in ponds where predators (invertebrates
and fish) and competitors were present
(IV), a result which intuitively seems
contradictory. However, not all amphibian
species avoid habitats with predatory fish
(e.g. Laurila & Aho 1997, Laurila 1998),
and also other studies have found positive
correlations with predator presence and
amphibian abundance and diversity
(Lehtinen et al. 1999, Babbitt et al. 2003,
Van Buskirk 2005). It is likely that these
16
positive correlations reflect the quality
of the habitats (Babbitt et al. 2003, Van
Buskirk 2005), hence avoiding predation
or competition may be less important than
finding a pond that fulfills other quality
requirements.
For a pond to be occupied by an
amphibian, it must be within the limits of
a species’ dispersal capability. In Finnish
agricultural landscapes, R. temporaria
abundance was positively linked to the
number of ditches and area of ponds in
the surrounding landscape (V), whereas
in Gotland, amphibian occurrence and
diversity correlated positively with the
proportion of wetlands and negatively
with the proportion of arable land in the
landscape surrounding breeding ponds
(IV). The positive relations with wetland
area likely reflect successful dispersal
and migration events between habitats
(Cushman 2006), which ensure population
persistence irrespective of variation in
other environmental factors (Hanski 1998,
Joly et al. 2001), but they may additionally
arise from enhanced likelihoods of finding
compensatory breeding and wintering
habitats when traditionally used habitats
are dry (Bowne et al. 2006). Parallel
positive relations between amphibians
and wetland area (Vos & Stumpel 1995,
Kolozsvary & Swihart 1999, Joly et al.
2001), and negative ones between arable
area (Joly et al. 2001, Beja & Alcazar
2003, Johansson et al. 2005) have been
observed in other amphibian studies in
farmland areas. These results give reason
to believe that amphibian populations may
be adversely affected by the expansion and
intensification of agriculture, particularly
by the loss of aquatic habitats, and that
in addition to preserving terrestrial
connectivity (Cushman 2006) also dense
wetland patterns should be remained to
ensure regional viability of amphibian
populations.
Main results and discussion
Temporal scale
Forests are often essential determinants
of amphibian distributions in agriculturedominated areas (Laan & Verboom 1990,
Joly et al. 2001, Guerry & Hunter 2002,
Porej et al. 2004), but this was not found for
amphibian occurrence in Gotland (IV) or
R. temporaria abundance in Finland during
normal weather conditions (V). However,
after a severe drought (and consequent
population crashes), R. temporaria
populations were more abundant in areas
where the neighboring landscape had more
forests (V). These results suggest that the
importance of forests for amphibians can
be context dependent and vary according
to climatic conditions. It is possible
that during the drought the agricultural
landscape became more hostile, and the
forests increased the migratory success
of adults (as they have been shown for
juvenile amphibians; Rothermel 2004),
and provided protection against drying.
Similarly, the area of cultivated land was
negatively associated with amphibian
abundance only after the drought (V).
Finnish agricultural landscape is a mosaic
of forests and cultivated habitats, which
may explain why the positive associations
with forest area and negative ones with
agricultural land arose only after the
drought.
R.
temporaria
populations
persisted during drought better in more
heterogeneous landscapes (V). Habitat
heterogeneity has been shown to promote
diversity, reduce the extinction risk
of populations in fragmented habitats
(Ricketts 2001), and buffer against the
impacts of agricultural intensification
(Donald & Evans 2006, see 1.1.). Our study
suggests that heterogeneity of agricultural
landscapes may furthermore enhance
population persistence during climatic
extremes (V). Our findings support the
view that habitat heterogeneity can dampen
the effects of environmental stochasticity
by decreasing the synchrony of population
fluctuations (Kindvall 1996, Sutcliffe et
al. 1997, McLaughlin et al. 2002), and
hence protect against variable climatic
conditions and enhance the maintenance
of populations (Ehrlich & Murphy 1987,
Kindvall 1996, Weiss et al. 1998). This can
have significant ramifications as extreme
events are likely to occur more frequently
as a part of the ongoing climate change
(Easterling et al. 2000, IPCC 2001).
To better understand present species
distributions in relation to land use
parameters, knowledge of past habitat
characteristics can be central (Swetnam et
al. 1999, Lunt & Spooner 2005). Historical
land use may affect the quality of presentday habitats (e.g. soil characteristics;
Honnay et al. 1999, Verheyen et al. 1999),
and present-day species distributions
may reflect past habitat circumstances
if populations have not yet responded to
habitat loss (a time lag in their responses;
Tilman et al. 1994, Kareiva & Wennergren
1995). This may lead to the situation where
species are present in habitats from which
they will go extinct in the future (e.g. Brooks
et al. 1999, Lindborg & Eriksson 2004,
Helm et al. 2006). In Gotland, amphibian
occurrences were negatively associated
with the historic proportion of arable land
in the surrounding landscape and positively
with historic forest area (IV). Although the
amount of unexplained variation in this
study was high, the results indicate that
areas with long agricultural histories may
be of poorer quality for amphibians, and
that agricultural expansion has negatively
impacted amphibian distributions in
Gotland. Additionally the results suggest
that the distribution patterns of amphibian
species are likely to reflect an interplay
between local and regional habitat quality
and historical land use.
17
Conclusions
4. Conclusions
Agricultural intensification has been
estimated to be one of the greatest threats
to biodiversity. In this thesis, I showed
that current-day agriculture can impact
amphibians in many, often negative ways.
Pesticide exposure decreased the survival,
and impeded the adaptive responses
of Rana temporaria tadpoles to biotic
stressors and increased the costs related
to these responses, hence decreasing their
fitness. Decreased fitness and survival
of tadpoles may affect the viability of
amphibian populations negatively, and for
R. temporaria, larval survival in particular
has been estimated to have a strong influence
on population dynamics (Biek et al. 2002).
However, as pointed out by e.g. Forbes et
al. (2001) and Schmidt (2004), the link
between individual-level and populationlevel responses is not straightforward,
because population-level effects may
be influenced by density-dependent,
compensatory responses. Keeping this in
mind, I argue that the results of my thesis
show that pesticides can interfere with key
processes in aquatic communities, and
affect the quality of surviving individuals.
How pesticide exposed juveniles cope
during their adulthood and whether e.g.
negative carryover effects on survival
and reproductive success can be seen
at later life stages, would need further
investigations.
I also demonstrated that agricultural
intensification may negatively impact the
occurrence of amphibians and decrease
their ability to persist during varying
climatic conditions. The results suggest that
in some cases, the costs of living in areas of
intensive agriculture may become apparent
only when other environmental stressors
are present. Maintaining heterogeneous
landscapes with enough wetlands would
18
seem to benefit amphibians in agricultural
landscapes. Many countries have adapted
agri-environment schemes, which aim
at reducing agrochemical emissions,
restoring landscapes and protecting
biodiversity (Klein & Sutherland 2003),
and e.g. organic farming and set-aside lands
have been shown to benefit biodiversity in
many areas (Van Buskirk & Willi 2004,
Hole et al. 2005). My results insinuate
that these farming practices could benefit
amphibians as well, and that their impacts
on amphibians would be an area of fruitful
future investigations.
The results obtained in my thesis
imply that for amphibians in agricultural
habitats, it is essential that there exists
enough wetlands adjacent to the breeding
sites. Recently it was shown that pond
quality does not explain the absence of
R. temporaria and Rana arvalis from
agricultural ponds in southern Sweden,
and focus on the quality of the terrestrial
habitat surrounding the ponds and the
metapopulation structure was suggested
to help in explaining the observed
phenomenon (Loman & Lardner 2006).
My results indicate that increased isolation
of breeding ponds caused by domination
of agricultural lands and loss of wetlands,
as well as habitat homogeneity are
characteristics that could partly explain
the absence of these amphibians in the
studied agricultural habitats. Due to the
importance of wetlands for amphibians,
future agricultural intensification is likely
to be an increasing threat to amphibian
populations, because more lands will
be drained and ponds filled, and also
because agricultural wetlands have not
been well protected in agri-environment
schemes (Bradbury & Kirby 2006). Small
constructed wetlands, which are used for
Conclusions
the controlling of agricultural runoff, have
been suggested as potential solutions for
maintaining aquatic habitats in agricultural
areas, and they have been estimated to be
suitable habitats for many farmland species
(Bradbury & Kirby 2006). However, I
believe some reservations about their
suitability are needed, as although these
habitats may well be used by many
farmland species, including amphibians,
they may also be sources of particularly
high pesticide concentrations. Hence,
maintaining aquatic habitats with sufficient
buffer strips is likely to be needed to ensure
with high water quality.
In summary, due to the pervasiveness
of modern-day agriculture and to the
fact that amphibian breeding habitats are
often situated in agricultural landscapes,
agriculture undoubtedly is a factor
influencing many amphibian populations.
By conserving wetlands, controlling for
the use of pesticides and by increasing
habitat heterogeneity, we may have a better
chance of maintaining viable amphibian
populations and greater biodiversity in
agricultural landscapes also in the future.
19
Acknowledgements
5. Acknowledgements
My warmest compliments go to the following:
The Gurus:
Juha Merilä, my mighty supervisor, I am forever grateful for these years. You gave me all the
freedom I wanted to carry out this work and supported me wholly in all the twists and turns of
the process. In one way or the other, you were always available when needed, and succeeded in
finding positive, when I thought things were falling apart. I’ve felt that you (for one reason or
another) really trust what I’m doing, and it has meant a lot to me.
Miska Luoto, my second supervisor – you have been a tremendous asset during this work. You
are extreme fun and full of ideas, and have opened a whole new world of landscape ecology for
me. I am grateful for that, and your endless support and encouragement. You have an excellent
ability to sense when I’m stressed and your frequent phone calls were just the thing needed to get
tricky issues quickly solved.
Anssi Laurila, your knowledge of tadpoles, phenotypic plasticity, lab experiments, and aquatic
ecology is astonishing; not to mention that you were once a Prince fan. These all have made
you an important person for me during this work, and extreme fun to talk to! Thank you for all
your input and effort, and for being so nicely laid back; you really help in putting things into
perspective and also finding the nitty-gritty of blurry results.
The University People:
A very big thankyou to all the current and former members of the EGRU crew, I’ve really enjoyed
your great company, humor and support. Likewise, I want to thank all the Uppsala frog people,
particularly Markus, Johan, and Mattias, for collaboration and fun times. Fredrik, Maarit, Susanna
and Céline - I have learned a lot from you work wise, but more than that I’m so happy to have
you as my friends. Also a biiiiig thanks to Ellu, Esa, Mari, Päivi, Minna and Dave for excellent
assistance with field and lab work. I’m sorry for the long hours. I’m grateful to Veijo Kaitala and
Ilkka Teräs for taking care of various study-related issues, Ullrika and Daniel with help building
up experiments, Annika Salama for help with finding a place for the experiments, Jouni Vainio
for computer assistance, and Leena Liikanen for being extremely helpful and patient with all
financial matters. I’d like to thank Mikko Kuussaari for letting me use the MYTVAS inventory
data, the ECRU group for letting me use their balance, Anne Aronta for help with making stock
solutions for pesticides, and Heino Vänskä for letting me use the yellow van during field seasons.
Hannu Pietiäinen, thank you for waking up an ecologist in me, Juha Tiainen and Ilpo Hanski for
giving an opportunity to do exhilarating field work, and thanks to all the inspiring teachers at
our department, and elsewhere, particularly Tuomo Mörä, Esa Väliverronen, and Hannu Rita.
Likewise, the fifth floor in Biocenter 3 has been a great place to work in - thanks to the pleasant
atmosphere created by all the PhD students and staff. I also want to thank my pre-examiners Rick
Relyea and David Skelly for constructive comments, and Heikki Kotiranta for commenting this
summary.
The Agri People:
I have spent many long days walking along ditches, and although it was nice per se, the people
that I met during these trips made all the difference. Thank you all for the wonderful discussions
and coffees, particularly Lahja and Oiva in Somero.
The Friends:
I’ve been lucky to find some of my best friends from Viikki: Inari, Jonna, and Katja - I’m so
happy I found you there. In your company no work day really feels like one; I’ll definitely miss
being in the same workplace with you. I’ve particularly loved our scientific discussions (e.g. on
the ingeniousness of 24 and Jack Bauer, and the many dimensions of Brad Pitt), which I hope
20
Acknowledgements
we’ll continue until the very end. K. erho: Foze, Hiiska, Säli (ja Imu), thank you for the relaxing
and fun times we’ve spent together, not to mention all the good food we’ve eaten. Foze, it’s been
great to share the frustrations and joys (?) of these last months with you! Outi, Gööran, Anna,
Ville, Pekka and Jukka - thanks for hilarious times during these years. I’m extremely thankful
to Sannamari, Katja and Suvi for not giving up on me, although I’ve been a lousy friend. Anna,
Anneli and the whole Starbo gang (Lilleman included) - thank you for your friendship and support
during these years, and for letting me use the Säkylä mökki during field work.
The Funding Agencies:
This work has been funded by The Maj and Tor Nessling Foundation, Oskar Öflund Foundation,
the Finnish Culture Foundation, and the Chancellor’s travel grants - thank you!
The Music:
During writing and long hours of car driving you’ve been the best of companies: Faith No More,
Incubus, Sadetanssi, Mike Stern, The Bad Plus, Prince, John Mayer, Bill Withers, the Younder
Mountain String Band, Queens of the Stone Age, Foo Fighters, Robbie Williams & Manic Street
Preachers.
The Non-Cited Literature:
I thank you for the thoughts: Paul Auster, Jonathan Franzen, Tom Robbins, Orhan Pamuk, Ian
McEwan, Franz K. & Fjodor D.
The Family:
Thank you äiti & iskä for all the support (financial and spiritual) and love during this project,
and thank you so much for taking care of Aarne, mom in particular. Thank you dad also for
giving me guidance in scientific thinking and structuring. I owe you both so much. Sanna Bobou,
my dear sister, I thank you for not being a scientist, and for being there for me always and for
understanding me (Did I leave the iron on?). A huge thanks to my parents-in-law Tuulikki and
Heikki for their support and interest in my work, and Tuulikki for taking care of Aarne. And of
course, a big thanks to the rest of the Valvanne and Piha families: Sudhir, Saara, Sani and Samu
for fun times
My Fellas: Markus and Aarne
Arska, my darling – you have changed my world completely, and brought so much laughter and
happiness that no setbacks have felt that bad knowing you’re around. I’m sorry for not being there
for you all the time. Olet äidin oma kulta.
Markus, my love, I’m so thankful for you for everything. Your knowledge of ecology, field work,
data analyses, and digitizing has helped me tremendously, and I’m really thankful for all the time
and thought you’ve put into my work, and for the discussions we’ve had about these issues. I’m
sorry for the stress during these last months, and that I’ve been so occupied with the work. Your
love and support have meant the world to me. I hope I can repay you when you finish your thesis.
This is how you both make me feel:
“When the day that lies ahead of me seems impossible to face.
When someone else instead of me always seems to know the way.
Then I look at you and the world’s alright with me.
Just one look at you and I know it’s gonna be - a lovely day.”
(Bill Withers)
21
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